The final frontier: ecological and evolutionary dynamics of a global parasite invasion

Abstract

Studying rapid biological changes accompanying the introduction of alien organisms into native ecosystems can provide insights into fundamental ecological and evolutionary theory. While powerful, this quasi-experimental approach is difficult to implement because the timing of invasions and their consequences are hard to predict, meaning that baseline pre-invasion data are often missing. Exceptionally, the eventual arrival of Varroa destructor (hereafter Varroa) in Australia has been predicted for decades. Varroa is a major driver of honeybee declines worldwide, particularly as vectors of diverse RNA viruses. The detection of Varroa in 2022 at over a hundred sites poses a risk of further spread across the continent. At the same time, careful study of Varroa's spread, if it does become established, can provide a wealth of information that can fill knowledge gaps about its effects worldwide. This includes how Varroa affects honeybee populations and pollination. Even more generally, Varroa invasion can serve as a model for evolution, virology and ecological interactions between the parasite, the host and other organisms.

Keywords: Apis; invasive species; mites; pollination; viruses.

Figure 1.

The three major expected impacts of Varroa on Australia's ecosystems. (a) Evolution. The recent incursion of Varroa into Australian naive honeybee populations enables evolutionary processes to be observed in both honeybees and Varroa. The use of anti-Varroa chemicals in hives, such as strips containing miticides, exposes Varroa to a selective pressure to adapt via miticide resistance mechanisms. The evolution of miticide resistance can contribute to our general understanding of adaptation, for the strength of selection (miticide concentration) will lead to different outcomes. For example, if the miticide concentration is not lethal to 100% of the original population, which has a normal distribution of viability (blue), the subsequent population will be formed from resistant individuals in the original population (yellow), with selection acting via the resistance phenotype on polygenic variation. At higher levels of miticide (dashed line), outside of the normal distribution of the original population. Selection will effectively act on rare mutations at single genes with a major impact on survival, over time leading to monogenic resistance (green) [14]. Similarly, bees and mites experience strong coevolutionary dynamics, providing general insights into this process. Monogenic and polygenic responses may occur in honeybees which facilitate natural adaptations to Varroa parasitism, or via artificial selective breeding programmes. This causes reciprocal genetic changes in the parasite and host over time. (b) Virology. Viral landscapes in bees change in the presence of Varroa. Mites facilitate a change in viral transmission route, leading to increased viral load and prevalence in honeybees. Viruses can spillover and impact viral landscapes in native bees that coexist in the same environments. As Varroa establishes and spreads, viral succession occurs with highly virulent viruses such as Black queen cell virus (BQCV) and Sacbrood virus (SBV) and Israeli acute paralysis virus/Kashmir bee virus (not shown) rapidly increasing, followed by Deformed wing virus (DWV) [8]. DWV is not yet established in Australia, which may result in unique outcomes if Varroa establishes in its absence. Tracking virus dynamics at the Varroa invasion front and over time in the colonized region, and observing viral load and disease emergence in honeybees and native bees will allow us to tease apart the relative influence of Varroa and viruses on bee health. (c) Ecology. The impact of Varroa on native and commercial ecosystems is largely driven by the removal of unmanaged honeybees, resulting in reduced pollination services. Pollination networks before and after Varroa establishment will change. Pollinators (left to right: commercial honeybee (Apis mellifera); unmanaged honeybee; native bees (Tetragonula sp.; Amegilla sp.; Hylaeus sp.; Exoneura sp.)) prior to Varroa are dominated by honeybees, but the near-complete removal of unmanaged bees after Varroa establishes will increase reliance on native bee pollination of crops and native plants (left to right: apple; tomato; dandelion; Leptospermum; Eucalyptus; native palm).